Antagonistic cytoprotective effects of C60 fullerene nanoparticles in simultaneous exposure to benzo[a]pyrene in a molluscan animal model.

Type Article
Date 2021-02
Language English
Author(s) Moore Michael N.1, 2, 3, Sforzini Susanna4, Viarengo Aldo4, Barranger Audrey1, Aminot YannORCID1, Readman James W.1, 3, Khlobystov Andrei N.5, 6, Arlt Volker M.7, 8, Banni Mohamed9, Jha Awadhesh N.1
Affiliation(s) 1 : School of Biological and Marine Sciences, University of Plymouth, Plymouth PL4 8AA, UK
2 : European Centre for Environment & Human Health (ECEHH), University of Exeter Medical School, Knowledge Spa, Royal Cornwall Hospital, Cornwall TR1 3LJ, UK
3 : Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth PL1 3HD, UK
4 : Institute for the study of Anthropic impacts and Sustainability in marine environment – IAS, National Research Council – CNR, Via de Marini, 6, 16149 Genova, GE, Italy
5 : School of Chemistry, University of Nottingham, University Park, Nottingham NG7 2RD, UK
6 : Nanoscale and Microscale Research Centre, University of Nottingham, University Park, Nottingham NG7 2RD, UK
7 : Kings Coll London, MRC PHE Ctr Environm & Hlth, Dept Analyt Environm & Forens Sci, London SE1 9NH, England
8 : Toxicology Department, GAB Consulting GmbH, 69126, Heidelberg, Germany
9 : Laboratory of Biochemistry and Environmental Toxicology, ISA, Chott-Mariem, Sousse, Tunisia
Source Science Of The Total Environment (0048-9697) (Elsevier BV), 2021-02 , Vol. 755 , N. 1 , P. 142355 (17p.)
DOI 10.1016/j.scitotenv.2020.142355
WOS© Times Cited 1
Keyword(s) Antagonism, Autophagy, Complexity, Lysosomes, C-60-nanoparticles, Oxidative-injury
Abstract

The hypothesis that C60 fullerene nanoparticles (C60) exerts an antagonistic interactive effect on the toxicity of benzo[a]pyrene (BaP) has been supported by this investigation. Mussels were exposed to BaP (5, 50 & 100 μg/L) and C60 (C60 - 1 mg/L) separately and in combination. Both BaP and C60 were shown to co-localise in the secondary lysosomes of the hepatopancreatic digestive cells in the digestive gland where they reduced lysosomal membrane stability (LMS) or increased membrane permeability, while BaP also induced increased lysosomal lipid and lipofuscin, indicative of oxidative cell injury and autophagic dysfunction. Combinations of BaP and C60 showed antagonistic effects for lysosomal stability, mTORC1 (mechanistic target of rapamycin complex 1) inhibition and intralysosomal lipid (5 & 50 μg/L BaP). The biomarker data (i.e., LMS, lysosomal lipidosis and lipofuscin accumulation; lysosomal/cell volume and dephosphorylation of mTORC1) were further analysed using multivariate statistics. Principal component and cluster analysis clearly indicated that BaP on its own was more injurious than in combination with C60. Use of a network model that integrated the biomarker data for the cell pathphysiological processes, indicated that there were significant antagonistic interactions in network complexity (% connectance) at all BaP concentrations for the combined treatments. Loss of lysosomal membrane stability probably causes the release of intralysosomal iron and hydrolases into the cytosol, where iron can generate harmful reactive oxygen species (ROS). It was inferred that this adverse oxidative reaction induced by BaP was ameliorated in the combination treatments by the ROS scavenging property of intralysosomal C60, thus limiting the injury to the lysosomal membrane; and reducing the oxidative damage in the cytosol and to the nuclear DNA. The ROS scavenging by C60, in combination with enhanced autophagic turnover of damaged cell constituents, appeared to have a cytoprotective effect against the toxic reaction to BaP in the combined treatments.

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Moore Michael N., Sforzini Susanna, Viarengo Aldo, Barranger Audrey, Aminot Yann, Readman James W., Khlobystov Andrei N., Arlt Volker M., Banni Mohamed, Jha Awadhesh N. (2021). Antagonistic cytoprotective effects of C60 fullerene nanoparticles in simultaneous exposure to benzo[a]pyrene in a molluscan animal model. Science Of The Total Environment, 755(1), 142355 (17p.). Publisher's official version : https://doi.org/10.1016/j.scitotenv.2020.142355 , Open Access version : https://archimer.ifremer.fr/doc/00652/76394/